Signaling mechanisms of angiotensin II-induced attenuation of GABAergic input to hypothalamic presympathetic neurons

Journal of Neurophysiology

Volumn 97, Issue 5, 2007, Pages 3279-3287

  Chen, Qian ^a,b   Pan, Hui Lin ^a,b  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOPYRIDINE; ANGIOTENSIN II; CADMIUM CHLORIDE; CALCIUM CHANNEL BLOCKING AGENT; CHELATING AGENT; DEFEROXAMINE; GUANINE NUCLEOTIDE BINDING PROTEIN; HYDROXYL RADICAL; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; PERTUSSIS TOXIN; PORPHYRIN DERIVATIVE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; SUPEROXIDE DISMUTASE; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; BICUCULLINE; MANGANESE(III) TETRAKIS(4 BENZOIC ACID)PORPHYRIN; MANGANESE(III)-TETRAKIS(4-BENZOIC ACID)PORPHYRIN; METALLOPORPHYRIN; POTASSIUM CHANNEL BLOCKING AGENT; UNCLASSIFIED DRUG;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CELL LABELING; CONTROLLED STUDY; DOWNSTREAM PROCESSING; FLUORESCENCE; GABAERGIC TRANSMISSION; HYPOTHALAMUS; MALE; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SYMPATHETIC NERVE CELL; WHOLE CELL; ANALYSIS OF VARIANCE; ANIMAL; ANTERIOR HYPOTHALAMUS; CYTOLOGY; DRUG EFFECT; DRUG INTERACTION; IN VITRO STUDY; INHIBITORY POSTSYNAPTIC POTENTIAL; LAMINECTOMY; METABOLISM; METHODOLOGY; PATCH CLAMP; PHYSIOLOGY; RADIATION EXPOSURE; SENSORY NERVE CELL; SPRAGUE DAWLEY RAT; SYNAPTOSOME;

4-AMINOPYRIDINE; ANALYSIS OF VARIANCE; ANGIOTENSIN II; ANIMALS; BICUCULLINE; DEFEROXAMINE; DRUG INTERACTIONS; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; INHIBITORY POSTSYNAPTIC POTENTIALS; LAMINECTOMY; MALE; METALLOPORPHYRINS; NEURONS, AFFERENT; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNEL BLOCKERS; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

EID: 34249865672     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01329.2006     Document Type: Article

References (63)

1. Allen AM. Inhibition of the hypothalamic paraventricular nucleus in spontaneously hypertensive rats dramatically reduces sympathetic vasomotor tone. Hypertension 39: 275-280, 2002.
2. Averill DB, Diz DI. Angiotensin peptides and baroreflex control of sympathetic outflow: pathways and mechanisms of the medulla oblongata. Brain Res Bull 51: 119-128, 2000.
3. Avshalumov MV, Chen BT, Rice ME. Mechanisms underlying H(2)O(2)-mediated inhibition of synaptic transmission in rat hippocampal slices. Brain Res 882: 86-94, 2000.
4. Bacal K, Kunze DL. Dual effects of angiotensin II on calcium currents in neonatal rat nodose neurons. J Neurosci 14: 7159-7167, 1994.
5. Bains JS, Ferguson AV. Paraventricular nucleus neurons projecting to the spinal cord receive excitatory input from the subfornical organ. Am J Physiol Regul Integr Comp Physiol 268: R625-R633, 1995.
6. Batinic-Haberle I, Benov L, Spasojevic I, Fridovich I. The ortho effect makes manganese(III) meso-tetrakis(N-methylpyridinium-2-yl)porphyrin a powerful and potentially useful superoxide dismutase mimic. J Biol Chem 273: 24521-24528, 1998.
7. Brown CH, Johnstone LE, Murphy NP, Leng G, Russell JA. Local injection of pertussis toxin attenuates morphine withdrawal excitation of rat supraoptic nucleus neurones. Brain Res Bull 52: 115-121, 2000.
8. Chan SH, Hsu KS, Huang CC, Wang LL, Ou CC, Chan JY. NADPH oxidase-derived superoxide anion mediates angiotensin II-induced pressor effect via activation of p38 mitogen-activated protein kinase in the rostral ventrolateral medulla. Circ Res 97: 772-780, 2005.
9. Chen Q, Li DP, Pan HL. Presynaptic alpha1 adrenergic receptors differentially regulate synaptic glutamate and GABA release to hypothalamic presympathetic neurons. J Pharmacol Exp Ther 316: 733-742, 2006.
10. Chen Q, Pan HL. Regulation of synaptic input to hypothalamic presympathetic neurons by GABA(B) receptors. Neuroscience 142: 595-606, 2006.
11. Consolim-Colombo FM, Hay M, Smith TC, Elizondo-Fournier M, Bishop VS. Subcellular mechanisms of angiotensin II and arginine vasopressin activation of area postrema neurons. Am J Physiol Regul Integr Comp Physiol 271: R34-R41, 1996.
12. Cooper EC, Milroy A, Jan YN, Jan LY, Lowenstein DH. Presynaptic localization of Kv1.4-containing A-type potassium channels near excitatory synapses in the hippocampus. J Neurosci 18: 965-974, 1998.
13. Coote JH, Yang Z, Pyner S, Deering J. Control of sympathetic outflows by the hypothalamic paraventricular nucleus. Clin Exp Pharmacol Physiol 25: 461-463, 1998.
14. Crawford KW, Frey EA, Cote TE. Angiotensin II receptor recognized by DuP753 regulates two distinct guanine nucleotide-binding protein signaling pathways. Mol Pharmacol 41: 154-162, 1992.
15. Day BJ, Fridovich I, Crapo JD. Manganic porphyrins possess catalase activity and protect endothelial cells against hydrogen peroxide-mediated injury. Arch Biochem Biophys 347: 256-262, 1997.
16. Erdos B, Broxson CS, King MA, Scarpace PJ, Tumer N. Acute pressor effect of central angiotensin II is mediated by NAD(P)H-oxidase-dependent production of superoxide in the hypothalamic cardiovascular regulatory nuclei. J Hypertens 24: 109-116, 2006.
17. Fields TA, Casey PJ. Signalling functions and biochemical properties of pertussis toxin-resistant G-proteins. Biochem J 321: 561-571, 1997.
18. Finnegan TF, Chen SR, Pan HL. Mu opioid receptor activation inhibits GABAergic inputs to basolateral amygdala neurons through Kv1.1/1.2 channels. J Neurophysiol 95: 2032-2041, 2006.
19. Gao L, Wang W, Li YL, Schultz HD, Liu D, Cornish KG, Zucker IH. Sympathoexcitation by central ANG II: roles for AT1 receptor upregulation and NAD(P)H oxidase in RVLM. Am J Physiol Heart Circ Physiol 288: H2271-H2279, 2005.
20. Gehlert DR, Gackenheimer SL, Schober DA. Autoradiographic localization of subtypes of angiotensin II antagonist binding in the rat brain. Neuroscience 44: 501-514, 1991.
21. Giniatullin AR, Darios F, Shakirzyanova A, Davletov B, Giniatullin R. SNAP25 is a pre-synaptic target for the depressant action of reactive oxygen species on transmitter release. J Neurochem 98: 1789-1797, 2006.
22. Griendling KK, Minieri CA, Ollerenshaw JD, Alexander RW. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res 74: 1141-1148, 1994.
23. Groemping Y, Lapouge K, Smerdon SJ, Rittinger K. Molecular basis of phosphorylation-induced activation of the NADPH oxidase. Cell 113: 343-355, 2003.
24. Gutkind JS, Kurihara M, Castren E, Saavedra JM. Increased concentration of angiotensin II binding sites in selected brain areas of spontaneously hypertensive rats. J Hypertens 6: 79-84, 1988.
25. Hadjiivanova CH, Georgiev V. In vitro effect of angiotensin II on GABA release in rat hippocampus. Neuropeptides 32: 431-434, 1998.
26. Ishikawa T, Nakamura Y, Saitoh N, Li WB, Iwasaki S, Takahashi T. Distinct roles of Kv1 and Kv3 potassium channels at the calyx of Held presynaptic terminal. J Neurosci 23: 10445-10453, 2003.
27. Jensen LL, Harding JW, Wright JW. Role of paraventricular nucleus in control of blood pressure and drinking in rats. Am J Physiol Renal Physiol 262: F1068-F1075, 1992.
28. Klann E, Roberson ED, Knapp LT, Sweatt JD. A role for superoxide in protein kinase C activation and induction of long-term potentiation. J Biol Chem 273: 4516-4522, 1998.
29. Kohno T, Kumamoto E, Higashi H, Shimoji K, Yoshimura M. Actions of opioids on excitatory and inhibitory transmission in substantia gelatinosa of adult rat spinal cord. J Physiol 518: 803-813, 1999.
30. Li DP, Chen SR, Finnegan TF, Pan HL. Signalling pathway of nitric oxide in synaptic GABA release in the rat paraventricular nucleus. J Physiol 554: 100-110, 2004.
31. Li DP, Chen SR, Pan HL. Angiotensin II stimulates spinally projecting paraventricular neurons through presynaptic disinhibition. J Neurosci 23: 5041-5049, 2003.
32. Li DP, Pan HL. Angiotensin II attenuates synaptic GABA release and excites paraventricular-rostral ventrolateral medulla output neurons. J Pharmacol Exp Ther 313: 1035-1045, 2005.
33. Li DP, Pan HL. Plasticity of GABAergic control of hypothalamic presympathetic neurons in hypertension. Am J Physiol Heart Circ Physiol 290: H1110-H1119, 2006a.
34. B receptors in paraventricular nucleus in control of sympathetic vasomotor tone in hypertension. J Pharmacol Exp Ther 320: 615-626, 2007.
35. Martin DS, Haywood JR. Hemodynamic responses to paraventricular nucleus disinhibition with bicuculline in conscious rats. Am J Physiol Heart Circ Physiol 265: H1727-H1733, 1993.
36. Mathie A, Wooltorton JR, Watkins CS. Voltage-activated potassium channels in mammalian neurons and their block by novel pharmacological agents. Gen Pharmacol 30: 13-24, 1998.
37. Mendelsohn FA, Chai SY, Dunbar M. In vitro autoradiographic localization of angiotensin-converting enzyme in rat brain using 125I-labelled MK351A. J Hypertens Suppl 2: S41-S44, 1984.
38. Miyakubo H, Hayashi Y, Tanaka J. Enhanced response of subfornical organ neurons projecting to the hypothalamic paraventricular nucleus to angiotensin II in spontaneously hypertensive rats. Auton Neurosci 95: 131-136, 2002.
39. Mohazzab KM, Kaminski PM, Wolin MS. NADH oxidoreductase is a major source of superoxide anion in bovine coronary artery endothelium. Am J Physiol Heart Circ Physiol 266: H2568-H2572, 1994.
40. Oldfield BJ, Davern PJ, Giles ME, Allen AM, Badoer E, McKinley MJ. Efferent neural projections of angiotensin receptor (AT1) expressing neurones in the hypothalamic paraventricular nucleus of the rat. J Neuroendocrinol 13: 139-146, 2001.
41. Pyner S, Coote JH. Identification of branching paraventricular neurons of the hypothalamus that project to the rostroventrolateral medulla and spinal cord. Neuroscience 100: 549-556, 2000.
42. Rodriguez-Puyol M, Griera-Merino M, Perez-Rivero G, Diez-Marques ML, Ruiz-Torres MP, Rodriguez-Puyol D. Angiotensin II induces a rapid and transient increase of reactive oxygen species. Antioxid Redox Signal 4: 869-875, 2002.
43. 2+ currents in rat nodose ganglion neurons. Neuroscience 85: 939-956, 1998.
44. Saad WA, Guarda IF, de Arruda Camargo LA, Dos Santos TA. L-Type calcium channels mediate water intake induced by angiotensin injection into median preoptic nucleus. Pharmacol Biochem Behav 83: 598-602, 2006.
45. Stahl GL, Pan HL, Longhurst JC. Activation of ischemia- and reperfusion-sensitive abdominal visceral C fiber afferents. Role of hydrogen peroxide and hydroxyl radicals. Circ Res 72: 1266-1275, 1993.
46. Strack AM, Sawyer WB, Hughes JH, Platt KB, Loewy AD. A general pattern of CNS innervation of the sympathetic outflow demonstrated by transneuronal pseudorabies viral infections. Brain Res 491: 156-162, 1989.
47. Swanson LW, Sawchenko PE. Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Annu Rev Neurosci 6: 269-324, 1983.
48. Takahashi T, Kajikawa Y, Tsujimoto T. G-Protein-coupled modulation of presynaptic calcium currents and transmitter release by a GABAB receptor. J Neurosci 18: 3138-3146, 1998.
49. Taniyama Y, Griendling KK. Reactive oxygen species in the vasculature: molecular and cellular mechanisms. Hypertension 42: 1075-1081, 2003.
50. + currents influence firing properties of isolectin B4-positive but not isolectin B4-negative primary sensory neurons. J Neurophysiol 93: 3401-3409, 2005.
51. 2+, and protein kinase C play a role in angiotensin II-induced free radical production in nucleus tractus solitarius. Hypertension 48: 482-489, 2006.
52. Wang G, Anrather J, Huang J, Speth RC, Pickel VM, Iadecola C. NADPH oxidase contributes to angiotensin II signaling in the nucleus tractus solitarius. J Neurosci 24: 5516-5524, 2004.
53. Wang Y, Floor E. Hydrogen peroxide inhibits the vacuolar H+-ATPase in brain synaptic vesicles at micromolar concentrations. J Neurochem 70: 646-652, 1998.
54. 2+ channel currents to a mu opioid in isolectin B4-positive and -negative dorsal root ganglion neurons. J Pharmacol Exp Ther 311: 939-947, 2004.
55. Wu ZZ, Pan HL. High voltage-activated Ca(2+) channel currents in isolectin B(4)-positive and -negative small dorsal root ganglion neurons of rats. Neurosci Lett 368: 96-101, 2004.
56. Yamamoto BK, Zhu W. The effects of methamphetamine on the production of free radicals and oxidative stress. J Pharmacol Exp Ther 287: 107-114, 1998.
57. Yang K, Fujita T, Kumamoto E. Adenosine inhibits GABAergic and glycinergic transmission in adult rat substantia gelatinosa neurons. J Neurophysiol 92: 2867-2877, 2004.
58. Zahner MR, Pan HL. Role of paraventricular nucleus in the cardiogenic sympathetic reflex in rats. Am J Physiol Regul Integr Comp Physiol 288: R420-R426, 2005.
59. Zhang ZH, Francis J, Weiss RM, Felder RB. The renin- angiotensinaldosterone system excites hypothalamic paraventricular nucleus neurons in heart failure. Am J Physiol Heart Circ Physiol 283: H423-H433, 2002.
60. Zhu M, Natarajan R, Nadler JL, Moore JM, Gelband CH, Sumners C. Angiotensin II increases neuronal delayed rectifier K(+) current: role of 12-lipoxygenase metabolites of arachidonic acid. J Neurophysiol 84: 2494-2501, 2000.
61. Zimmerman MC, Dunlay RP, Lazartigues E, Zhang Y, Sharma RV, Engelhardt JF, Davisson RL. Requirement for Rac1-dependent NADPH oxidase in the cardiovascular and dipsogenic actions of angiotensin II in the brain. Circ Res 95: 532-539, 2004.
62. Zimmerman MC, Lazartigues E, Lang JA, Sinnayah P, Ahmad IM, Spitz DR, Davisson RL. Superoxide mediates the actions of angiotensin II in the central nervous system. Circ Res 91: 1038-1045, 2002.
63. Zimmerman MC, Sharma RV, Davisson RL. Superoxide mediates angiotensin II-induced influx of extracellular calcium in neural cells. Hypertension 45: 717-723, 2005.